Long-range dispersal and high-latitude environments influence the population structure of a "stress-tolerant" dinoflagellate endosymbiont.

Pettay DT, Lajeunesse TC - PLoS ONE (2013)

Bottom Line:
In contrast to its host, however, subtropical populations of S. glynni in the Gulf of California (Sea of Cortez) were strongly differentiated from populations in tropical eastern Pacific.We infer that S. glynni genotypes harbored by host larvae arriving from more southern locations are rapidly replaced by genotypes adapted to more temperate environments.The strong population structure of S. glynni corresponds with fluctuating environmental conditions and suggests that these genetically diverse populations have the potential to evolve rapidly to changing environments and reveals the importance of environmental extremes in driving microbial eukaryote (e.g., plankton) speciation in marine ecosystems.

Affiliation: Department of Biology, Pennsylvania State University, University Park, Pennsylvania, United States of America ; College of Earth, Ocean, and Environment, University of Delaware, Lewes, Delaware, United States of America.

ABSTRACTThe migration and dispersal of stress-tolerant symbiotic dinoflagellates (genus Symbiodinium) may influence the response of symbiotic reef-building corals to a warming climate. We analyzed the genetic structure of the stress-tolerant endosymbiont, Symbiodinium glynni nomen nudum (ITS2 - D1), obtained from Pocillopora colonies that dominate eastern Pacific coral communities. Eleven microsatellite loci identified genotypically diverse populations with minimal genetic subdivision throughout the Eastern Tropical Pacific, encompassing 1000's of square kilometers from mainland Mexico to the Galapagos Islands. The lack of population differentiation over these distances corresponds with extensive regional host connectivity and indicates that Pocillopora larvae, which maternally inherit their symbionts, aid in the dispersal of this symbiont. In contrast to its host, however, subtropical populations of S. glynni in the Gulf of California (Sea of Cortez) were strongly differentiated from populations in tropical eastern Pacific. Selection pressures related to large seasonal fluctuations in temperature and irradiance likely explain this abrupt genetic discontinuity. We infer that S. glynni genotypes harbored by host larvae arriving from more southern locations are rapidly replaced by genotypes adapted to more temperate environments. The strong population structure of S. glynni corresponds with fluctuating environmental conditions and suggests that these genetically diverse populations have the potential to evolve rapidly to changing environments and reveals the importance of environmental extremes in driving microbial eukaryote (e.g., plankton) speciation in marine ecosystems.

pone-0079208-g001: Structure plot of S. glynni populations from the tropical and subtropical eastern Pacific.Structure plot of S. glynni populations based on allelic frequencies at 11 microsatellite loci. Each bar in the graph represents the probability that a sample belongs to a particular color-coded population. Each graph represents analyses for a particular number of populations (K) run under an admixture with a correlated allele frequency model. (a) Major differentiation occurred between the Gulf of California population and populations in the ETP (k = 2). (b) Additional clustering occurred in the ETP, yet did not correspond to location, depth or host morphospecies (k = 3).

Mentions:
Two well supported populations were detected using the Evanno et al. method to process the Structure results (k = 2; ln P(D) = -2351.4; Figure 1, Figure S1), and corresponded to the subtropical GoC region and the ETP (Figure 2). The posterior probabilities for increasing values of K continued to rise until k = 6, at which they stabilize and/or decline (Figure S1). Further examination of Structure runs at k = 3 showed consistency between runs and additional structuring within the ETP region and may represent two cryptic populations within the region (Figure 1; ln P(D) = -2230.4 & Δruns = 1.0; Figure S1); however, this additional subdivision appeared haphazard and does not relate to geographic location or depth. Subsequent analyses on the ETP region only, and using the location prior feature, revealed similar patterns as above with no further subdivision in relation to geographic location in the ETP (data not shown). Additional analyses using BAPS supported the two regional populations (k = 2; log(ml) = -2489.7) with no further subdivision of the ETP, even when analyzed in isolation (k = 1; log(ml) = -1780.3).

pone-0079208-g001: Structure plot of S. glynni populations from the tropical and subtropical eastern Pacific.Structure plot of S. glynni populations based on allelic frequencies at 11 microsatellite loci. Each bar in the graph represents the probability that a sample belongs to a particular color-coded population. Each graph represents analyses for a particular number of populations (K) run under an admixture with a correlated allele frequency model. (a) Major differentiation occurred between the Gulf of California population and populations in the ETP (k = 2). (b) Additional clustering occurred in the ETP, yet did not correspond to location, depth or host morphospecies (k = 3).

Mentions:
Two well supported populations were detected using the Evanno et al. method to process the Structure results (k = 2; ln P(D) = -2351.4; Figure 1, Figure S1), and corresponded to the subtropical GoC region and the ETP (Figure 2). The posterior probabilities for increasing values of K continued to rise until k = 6, at which they stabilize and/or decline (Figure S1). Further examination of Structure runs at k = 3 showed consistency between runs and additional structuring within the ETP region and may represent two cryptic populations within the region (Figure 1; ln P(D) = -2230.4 & Δruns = 1.0; Figure S1); however, this additional subdivision appeared haphazard and does not relate to geographic location or depth. Subsequent analyses on the ETP region only, and using the location prior feature, revealed similar patterns as above with no further subdivision in relation to geographic location in the ETP (data not shown). Additional analyses using BAPS supported the two regional populations (k = 2; log(ml) = -2489.7) with no further subdivision of the ETP, even when analyzed in isolation (k = 1; log(ml) = -1780.3).

Bottom Line:
In contrast to its host, however, subtropical populations of S. glynni in the Gulf of California (Sea of Cortez) were strongly differentiated from populations in tropical eastern Pacific.We infer that S. glynni genotypes harbored by host larvae arriving from more southern locations are rapidly replaced by genotypes adapted to more temperate environments.The strong population structure of S. glynni corresponds with fluctuating environmental conditions and suggests that these genetically diverse populations have the potential to evolve rapidly to changing environments and reveals the importance of environmental extremes in driving microbial eukaryote (e.g., plankton) speciation in marine ecosystems.

Affiliation:
Department of Biology, Pennsylvania State University, University Park, Pennsylvania, United States of America ; College of Earth, Ocean, and Environment, University of Delaware, Lewes, Delaware, United States of America.

ABSTRACTThe migration and dispersal of stress-tolerant symbiotic dinoflagellates (genus Symbiodinium) may influence the response of symbiotic reef-building corals to a warming climate. We analyzed the genetic structure of the stress-tolerant endosymbiont, Symbiodinium glynni nomen nudum (ITS2 - D1), obtained from Pocillopora colonies that dominate eastern Pacific coral communities. Eleven microsatellite loci identified genotypically diverse populations with minimal genetic subdivision throughout the Eastern Tropical Pacific, encompassing 1000's of square kilometers from mainland Mexico to the Galapagos Islands. The lack of population differentiation over these distances corresponds with extensive regional host connectivity and indicates that Pocillopora larvae, which maternally inherit their symbionts, aid in the dispersal of this symbiont. In contrast to its host, however, subtropical populations of S. glynni in the Gulf of California (Sea of Cortez) were strongly differentiated from populations in tropical eastern Pacific. Selection pressures related to large seasonal fluctuations in temperature and irradiance likely explain this abrupt genetic discontinuity. We infer that S. glynni genotypes harbored by host larvae arriving from more southern locations are rapidly replaced by genotypes adapted to more temperate environments. The strong population structure of S. glynni corresponds with fluctuating environmental conditions and suggests that these genetically diverse populations have the potential to evolve rapidly to changing environments and reveals the importance of environmental extremes in driving microbial eukaryote (e.g., plankton) speciation in marine ecosystems.